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Supermonkey of the Americas

Paleontologists reconstruct the versatile lifestyle of Cartelles coimbrafilhoi, the largest simian ever to inhabit the continent

Sandro CastelliMore than 15,000 years ago, the area that is now Brazil was home to a monkey twice as large as the muriqui, or woolly spider monkey, the largest monkey living today in the New World. Evidence of the existence of this supermonkey of the Americas can be seen in a nearly complete fossil skeleton, discovered in 1992 in a cave in the municipality of Campo Formoso, in the Brazilian state of Bahia. Described by paleontologist Cástor Cartelle, who is now a researcher at Pontifical Catholic University of Minas Gerais (PUC-Minas), the supermonkey fossil was examined in detail more recently by Lauren Halenar and Alfred Rosenberger, paleontologists at the City University of New York (CUNY). Halenar and Rosenberger determined that the species—this year given the name Cartelles coimbrafilhoi—explored the forest floor much like a chimpanzee. At the same time, this large monkey, despite its large size, could climb trees and hang from branches with the same skill, if not quite the same speed, as the smaller species of its family, the Atelidae. Other members of this family are the howler monkey, the spider monkey, the big-bellied woolly monkey and the muriqui. “Cartelles probably moved and behaved unlike any other species of New World monkey living today,” Halenar says.

According to the researchers, the Cartelles coimbrafilhoi fossil is of key importance in reconstructing the little-known evolutionary history of the monkeys of this region. The classification of this fossil as a new species—actually, genus and species—brings to four the number of now-extinct monkey species that lived in South America in the late Pleistocene. The discovery of new fossils, such as those found in recent years by Rosenberger and colleagues in underwater caves in the Dominican Republic, should help complete the picture. Another important piece of the puzzle is the monkey found in Campo Formoso in 1992.

That year, while exploring a small section of the Toca da Boa Vista cave system, which at 100 kilometers long is considered the largest cave in the Southern hemisphere, a team of speliologists found one of the skeletons and informed Cartelle and his group. They found two fossil monkey skeletons that were fairly complete, with more than 90% of the bones preserved. The animals likely lived in fields and forests around the cave sometime between 360,000 and 15,000 years ago, at the end of the geological period known as the Pleistocene. Shortly after the animals died, their carcasses were probably swept into the cave by torrents of rushing water, and their bones were preserved there. “Finding a nearly complete skeleton from any taxon [group of organisms] is very rare,” Halenar comments.

The first descriptions of these fossils were published in 1996, in two scientific articles written by Cartelle and American paleontologist Walter Hartwig of Touro University in California. The skeleton described in the journal Proceedings of the National Academy of Sciences (PNAS) did not present much of a challenge. Subsequent studies confirmed that the species, named Caipora bambuiorum, was a larger version of the present-day spider monkey. Although it weighed about 20 kilos (twice that of a spider monkey), Caipora likely moved in a very similar fashion, able to use its arms and legs, as well as its prehensile tail, to swing nimbly among the tree branches.

The other skeleton, described by Hartwig and Cartelle in Nature, was more enigmatic. The researchers concluded that the most probable hypothesis was that it was a second fossil of a species discovered a century and a half earlier in a cave in the municipality of Lagoa Santa, in the state of Minas Gerais, more than 1,200 kilometers from Toca da Boa Vista. Danish paleontologist Peter Lund had found a fragment of a femur and a piece of arm bone in Lagoa Santa in 1836, and identified them as the first primate fossils ever discovered. Protopithecus brasiliensis is mentioned by Charles Darwin in his classic 1859 work, On the Origin of Species, and more recent estimates suggest that it weighed as much as 24 kilos.

Ana Paula CamposNevertheless, Cartelle says he had always suspected that some confirmation was needed as to whether the two fossils were really Protopithecus. He and Hartwig had compared the skeleton from Toca da Boa Vista with photos of the Protopithecus brasiliensis fragments kept at the Natural History Museum of Denmark. The two researchers had noticed small differences between the fossils, but interpreted them as natural variations among individuals of the same species. “He and I both thought we would go to Denmark some day for a better look,” says Cartelle, who has not yet had the opportunity to make the trip.

The hypothetical Protopithecus from Toca da Boa Vista also had a very odd combination of features, the researchers thought. During her doctoral studies completed in 2005, biologist Patrícia Guedes of the National Museum at the Federal University of Rio de Janeiro concluded that the fossil’s dentition, though somewhat worn, showed characteristics of two subfamilies of Atelidae: Alouattinae and Atelinae. She also observed that the shape of the skull was similar to that of the other Alouattinae, the subfamily in which howler monkeys are classified, while their teeth looked more like those of the subfamily Atelinae, to which the spider monkey, the big-bellied woolly monkey and the muriqui belong. Other studies of the skull and the rest of the body also suggested that the species had a mixture of features of those two subfamilies, separated more than 12.9 million years ago.

To attempt to resolve these contradictions, Rosenberger suggested to Halenar, who was then his doctoral student, that she devote her thesis to fully examining the P. brasiliensis fossils from Lagoa Santa and Toca da Boa Vista. Over the course of a few weeks spent in Copenhagen and Belo Horizonte, she measured the shapes and dimensions of the fossilized bones and then compared them with the bones of hundreds of individuals from several species of monkeys currently in the collection of the American Museum of Natural History in New York. The objective was to determine where the fossils fit in the phylogenetic tree of monkeys and to deduce how they moved, based on the shape of their bones. “We inferred the function of the elements of skeletons of extinct species by comparing the shape of their bones with those of living species,” Halenar explains.

“Halenar immediately noticed that some of the bones were anatomically very different,” Rosenberger recalls. In an article published in October 2013 in the Journal of Human Evolution, Rosenberger and Halenar propose that each of the fossils attributed to Protopithecus brasiliensis actually belongs to a different species.

The P. brasiliensis from Lagoa Santa, the researchers say, was likely an Atelinae. Although it is difficult to say anything more comprehensive about it on the basis of two bone fragments, Halenar believes that the species looked like a muriqui, but twice the size. The skeleton from Toca da Boa Vista was from the same subfamily as howler monkeys but belonged to a different genus. That species was given the name Cartelles coimbrafilhoi, in homage to Cartelle, who has been studying the mammals of the Brazilian Pleistocene for 50 years—at least four extinct species bear his name—and to Adelmar Coimbra-Filho, one of the pioneers of Brazilian primatology, who took action to save the golden lion tamarin from extinction.

Halenar estimates that Cartelles coimbrafilhoi weighed 25 to 28 kilos, which makes it the biggest of the four species of large monkeys that lived in Pleistocene America. C. coimbrafilhoi measured 1.67 meters from the top of its head to the tip of its tail, and the base of its skull and the mandible suggest those of a big-bellied woolly monkey. But the general shape of the skull looks like that of a howler monkey, including the same large space near the throat that houses the vocal apparatus of these monkeys, whose howls that can be heard at a distance of up to five kilometers. Halenar explains, however, that it is impossible to know whether C. coimbrafilhoi’s howls were as loud or louder than those of howler monkeys, because there is no simple correlation between their size and the intensity of their call. The social habits of each species and the environment in which they live also play a role.

The rest of the skeleton resembles that of a spider monkey, but more robust. The shape of its bones suggests a well-developed musculature, adapted for climbing and hanging. Hartwig and Cartelle had already posited that the animal likely felt at home in the treetops. But because of its size, some researchers dismissed the idea and suggested that the species lived only on the ground. As a general rule, only the smaller species tend to live an arboreal lifestyle, since the larger animals are at greater risk of breaking a branch and falling. But that is not always true. “Most arboreal New World monkeys weigh about 10 kilos,” explains primatologist Stephen Ferrari of the Federal University of Sergipe. “But an orangutan, the largest arboreal primate, can weigh as much as 100 kilos.”

In addition to being considerably smaller than an orangutan, Cartelles coimbrafilhoi may have also been helped by its thick, long tail to hold onto branches, although biomechanical studies are still needed to confirm whether its tail could be used as a fifth prehensile member to enable it to hang from branches and sustain the animal’s full weight, as in the case of several extant species of the Atelidae family.

In any event, the bones also indicate that the species had well-developed terrestrial habits. “It seems likely that Cartelles’ behavior was more akin to that of present-day chimpanzees, which are skillful climbers but spend most of their time on the ground,” Ferrari suggests. Guedes concurs, pointing out that even howler monkeys and muriquis, which are normally tree-dwellers, sometimes explore the ground. The team headed by primatologist Karen Strier of the University of Wisconsin-Madison recently wrote about the development of terrestrial habits among Northern muriquis living in a protected private reserve in Minas Gerais. In an article published in 2012 in Plos One, Strier maintains that the behavioral change is linked to an increase in the population, which has grown from 60 to 300 individuals in the past 30 years, and to the lack of sufficient space for so many monkeys in the reserve. According to Strier, as they learned to explore the ground, the muriquis found more food, so there was an increase in the birth rate, although the creatures have also become more vulnerable to predator attacks.

The four extinct species of Brazilian monkeys—Cartelles coimbrafilhoi, Caipora bambuiorum, Protopithecus brasiliensis and Alouatta mauroi—lived with the megafauna, large mammals such as giant sloths and sabre-toothed tigers, that inhabited the Americas in the Pleistocene and may have become extinct due to climate change. “Large primate species are much more vulnerable to extinction, regardless of the cause,” Halenar explains.

To date, there is no way of knowing whether a particular extant species of monkey is descended from the line of any of these very large animals. “The work done by Halenar and Rosenberger shines a spotlight on the dearth of available data on the postcranial morphology of American primates,” Guedes comments. “Understanding the variations in morphology of platyrhines [a group that includes New World monkeys with widely separated nostrils that open to the side] is key to hypothesizing relationships among them and to understanding the diversification of these mammals in South America.”

A good way to end the year

Team found two primate fossils just before a new year dawned

Ricardo Zorzetto 

Photographer Adriano Gambarini captured this photo of Cartelle and his two colleagues as they gathered fossils in  Toca da Boa Vista in 1992.

ADRIANO GAMBARINIPhotographer Adriano Gambarini captured this photo of Cartelle and his two colleagues as they gathered fossils in Toca da Boa Vista in 1992.ADRIANO GAMBARINI

The year 1992 had practically come to a close when Cástor Cartelle, a paleontologist specializing in extinct sloths, made one of the most important discoveries in Brazilian primatology. It was December 30, and he and two colleagues had walked for two hours through a labyrinth of tunnels, narrow passageways and abysses to reach a large chamber in the Toca da Boa Vista cave. There they found, side by side, the fossils of two of the largest species of monkeys that lived in the Americas in the late Pleistocene. “I thought at first that they were a male and a female,” says Cartelle, who would later learn that the fossils belonged to different species that had not yet been described.

He and his colleagues, Mauro Ferreira and Rodrigo Lopes Ferreira, did not get there by themselves. The day before, four or five members of the Bambuí Speleological Research Group, a large team that had been mapping Toca da Boa Vista for several years, had begun to explore a section of the cave called the “other world,” spotted the fossils and brought a sample to the camp, a school in Laje dos Negros, in the district of Campo Formoso. “Someone—I can’t remember who—brought a skull and showed it to us,” recalls Rodrigo Lopes Ferreira, who at the time was a biology student at the Federal University of Minas Gerais (UFMG) working with Cartelle. “We saw it was a monkey and we asked them to take us to the place where they’d found it.”

At right, one of the rooms in the cave

ADRIANO GAMBARINIAt right, one of the rooms in the caveADRIANO GAMBARINI

The researchers had a surprise when they came across the fossils on December 30. “One was five meters from the other, and their state of preservation was impressive,” he recalls. For more than eight hours, Cartelle and Mauro Ferreira examined the floor of the site, collecting everything they could find of the monkey skeletons, later described as Caipora bambuiorum and Protopithecus brasiliensis (the latter has now been renamed Cartelles coimbrafilhoi), and from a sloth fossil. Replicas of the skeletons will be on display at the PUC-Minas Museum of Natural Science, reopening in December 2013 after a 2012 fire.

At the time the monkeys lived, the area around Campo Formoso hosted a humid tropical forest that had been created as a result of contact between Atlantic and Amazonian vegetation. At the end of the last ice age, the regional climate became semiarid. On the day of the sample collection, the heat and dryness of the area were exacerbated by the high temperatures in the cave. “We spent a day in Purgatory’s waiting room,” Cartelle comments. “I’ve never sweated so much.” Even he, a non-drinker, had a beer or two that afternoon to celebrate.

Scientific article
HALENAR, L. B. and ROSENBERGER, A. L. A closer look at the “Protopithecus” fossil assemblages: new genus and species from Bahia, Brazil. Journal of Human Evolution. v. 65, n.4, p. 374-90. Oct. 2013.